Phylogenomics reveals extensive misidentification of fungal strains from the genus Aspergillus

Author:

Steenwyk Jacob L.123ORCID,Balamurugan Charu23,Raja Huzefa A.4ORCID,Gonçalves Carla23,Li Ningxiao56ORCID,Martin Frank6,Berman Judith7ORCID,Oberlies Nicholas H.4ORCID,Gibbons John G.8910ORCID,Goldman Gustavo H.11ORCID,Geiser David M.12,Houbraken Jos13,Hibbett David S.14ORCID,Rokas Antonis2315ORCID

Affiliation:

1. Howards Hughes Medical Institute and the Department of Molecular and Cell Biology, University of California, Berkeley, California, USA

2. Department of Biological Sciences, Vanderbilt University, Nashville, Tennessee, USA

3. Evolutionary Studies Initiative, Vanderbilt University, Nashville, Tennessee, USA

4. Department of Chemistry and Biochemistry, University of North Carolina at Greensboro, Greensboro, North Carolina, USA

5. Department of Plant Pathology, University of California, Davis, California, USA

6. USDA-ARS, Salinas, California, USA

7. Shmunis School of Biomedicine and Cancer Research, George S. Wise Faculty of Life Sciences, Tel Aviv University, Ramat Aviv, Israel

8. Department of Food Science, University of Massachusetts, Amherst, Massachusetts, USA

9. Molecular and Cellular Biology Graduate Program, University of Massachusetts, Amherst, Massachusetts, USA

10. Organismic and Evolutionary Biology Graduate Program, University of Massachusetts, Amherst, Massachusetts, USA

11. Faculdade de Ciencias Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, São Paulo, Brazil

12. Department of Plant Pathology and Environmental Microbiology, Penn State University, University Park, Pennsylvania, USA

13. Food and Indoor Mycology, Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands

14. Biology Department, Clark University, Worcester, Massachusetts, USA

15. Heidelberg Institute for Theoretical Studies, Schloss-Wolfsbrunnenweg, Heidelberg, Germany

Abstract

ABSTRACT Modern taxonomic classification is often based on phylogenetic analyses of a few molecular markers, although single-gene studies are still common. Here, we leverage genome-scale molecular phylogenetics (phylogenomics) of species and populations to reconstruct evolutionary relationships in a dense data set of 710 fungal genomes from the biomedically and technologically important genus Aspergillus . To do so, we generated a novel set of 1,362 high-quality molecular markers specific for Aspergillus and provided profile Hidden Markov Models for each, facilitating their use by others. Examining the resulting phylogeny helped resolve ongoing taxonomic controversies, identified new ones, and revealed extensive strain misidentification (7.59% of strains were previously misidentified), underscoring the importance of population-level sampling in species classification. These findings were corroborated using the current standard, taxonomically informative loci. These findings suggest that phylogenomics of species and populations can facilitate accurate taxonomic classifications and reconstructions of the Tree of Life. IMPORTANCE Identification of fungal species relies on the use of molecular markers. Advances in genomic technologies have made it possible to sequence the genome of any fungal strain, making it possible to use genomic data for the accurate assignment of strains to fungal species (and for the discovery of new ones). We examined the usefulness and current limitations of genomic data using a large data set of 710 publicly available genomes from multiple strains and species of the biomedically, agriculturally, and industrially important genus Aspergillus . Our evolutionary genomic analyses revealed that nearly 8% of publicly available Aspergillus genomes are misidentified. Our work highlights the usefulness of genomic data for fungal systematic biology and suggests that systematic genome sequencing of multiple strains, including reference strains (e.g., type strains), of fungal species will be required to reduce misidentification errors in public databases.

Funder

National Science Foundation

Life Sciences Research Foundation

HHS | NIH | National Institute of Allergy and Infectious Diseases

Publisher

American Society for Microbiology

Reference94 articles.

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